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Chapter 11 : Developmental Aggregation and Fruiting Body Formation in the Gliding Bacterium

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Abstract:

This chapter discusses what is perhaps the most unique facet of myxobacterial morphogenesis, the formation of multicellular aggregates and fruiting bodies by the cooperative action of tens of thousands of individual cells. The induction of fruiting body formation presumably requires two separate events. First, individual cells must monitor their own nutrient status. Second, each cell must evaluate the nutritional status and size of the entire population. Both mutants show identical developmental aggregation defects, suggesting that the Dif proteins probably do constitute a new signal transduction pathway necessary for aggregation during fruiting body formation, although no biochemical evidence is yet available to show that these proteins participate in such a pathway. Temporal aspects of fruiting body formation in have received little direct attention, although the conversion of vegetative cells into spores is certainly delayed under normal starvation conditions until the cells are within developmental aggregates. Several genes that may be involved with regulating the timing of fruiting body formation itself have also been identified. Cells which cannot synthesize protein myxobacterial Hemagglutinin (MBHA) show delayed aggregation, suggesting that MBHA may be required to increase the efficiency of cell-cell interactions and fruiting body formation. Studies of development suggest that temperature could play an important role in the developmental aggregation process. In recent years many advances have been made to our understanding of the developmental aggregation process.

Citation: Ward M, Zusman D. 2000. Developmental Aggregation and Fruiting Body Formation in the Gliding Bacterium , p 243-262. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch11
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Figures

Image of FIGURE 2
FIGURE 2

Gene organizations within motility- and directed-motility-associated loci. (A) locus (GenBank accession no. AF076485); (B) locus (accession no. AF049107, U47814, J04157, M35192, M35200, and U44437); (C) locus (accession no. AF047554); (D) locus (accession no. AF003632, L39904, and L78131). Genes which when mutated result in the frizzy aggregation phenotype during development are shown in dark gray. Restriction enzyme sites: B, HI; C, I (shown for the region only); P, I; and S, I. Arrows designate direction of transcription of genes.

Citation: Ward M, Zusman D. 2000. Developmental Aggregation and Fruiting Body Formation in the Gliding Bacterium , p 243-262. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch11
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FIGURE 3

Information flow through the enteric chemotaxis system. Chemical stimuli are sensed by the transmembrane MCP receptor proteins. Excitation signals are relayed via CheW to the histidine protein kinase CheA. CheA can both autophosphorylate and, when stimulated by the MCPs, phosphorylate CheY. CheY-P then interacts with the switch proteins of the flagellar motor, regulating the direction of flagellar rotation. Dephosphorylation of CheY-P is stimulated by CheZ, while adaptation to stimuli requires methylation and demethylation of the MCPs by CheR and CheB, respectively.

Citation: Ward M, Zusman D. 2000. Developmental Aggregation and Fruiting Body Formation in the Gliding Bacterium , p 243-262. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch11
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FIGURE 4

Alignment of CheY-like proteins from with CheY from . (a) Alignment of the CheY homologies in the DifD ( ), FrzE ( ), and FrzZ ( ) proteins against CheY ( ). The phosphorylation site ( Asp57) and associated amino acids are marked with “*.” Amino acids proposed to be involved with switch protein interactions are indicated with “” (b) Dendrogram created from the CheY protein alignment.

Citation: Ward M, Zusman D. 2000. Developmental Aggregation and Fruiting Body Formation in the Gliding Bacterium , p 243-262. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch11
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FIGURE 1

Wild-type and mutant developmental-aggregation phenotypes. (a) Strain DZ2 (wild type), shown developing at high cell numbers (2 × 10 CFU/ml) after 48 h of incubation at 34°C; (b) SW505 (; signal transduction mutant), showing formation of only small mounds after 48 h of incubation; (c) DK2630 (; extracellular-signaling mutant), showing formation of only small mounds after 24 h of development; (d) DZF3558 ( Δ; signal transduction mutant), showing the characteristic frizzy phenotype in the strain FB background after 72 h of incubation; (e) DZF1 (; ECF sigma factor mutant), showing trails of aggregates rather than discrete mounds after 24 h of development; (f) DZF1 (; signal transduction mutant), showing many small, closely spaced aggregates (photo courtesy of K. Cho); (g) DZ2 (; temperature-dependent aggregation mutant), showing no aggregation at 34°C (provided by K. O'Connor); (h) DZ2 () showing wild-type aggregation at 28°C (provided by K. O'Connor). All cells were plated on CF starvation agar ( ).

Citation: Ward M, Zusman D. 2000. Developmental Aggregation and Fruiting Body Formation in the Gliding Bacterium , p 243-262. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch11
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Image of FIGURE 5
FIGURE 5

Model showing the proposed interactions within the Frz signal transduction pathway during developmental aggregation. Components of the pathway that when mutated result in cells displaying the frizzy aggregation phenotype are colored dark gray. The FrzZ and AbcA proteins are suggested to act upstream of the central components, FrzCD, FrzA, and FrzE, and may regulate the export of a developmentally important molecule. This molecule might be modified or might modify a signal associated with late developmental aggregation. The histidine protein kinase (HPK) that phosphorylates FrzZ is unknown. However, FrzZ is proposed to potentially interact with the RpoEl protein to regulate gene expression. Inputs to the FrzCD receptor may be associated with the C-signaling pathway as well as with the AbcA-associated pathway. Other, unknown inputs may also occur. The role of FrzB is unknown, although the protein is suggested to interact with FrzCD. The FrzF and FrzG proteins methylate and demethylate FrzCD. It is also suggested that FrzF may interact with an unknown regulatory protein. The FrzS protein may be phosphorylated by FrzE and interact directly with the S-motility system. Likely pathways or interactions are shown connected by black arrows. More speculative interactions are shown connected by gray arrows.

Citation: Ward M, Zusman D. 2000. Developmental Aggregation and Fruiting Body Formation in the Gliding Bacterium , p 243-262. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch11
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Image of FIGURE 6
FIGURE 6

Electron micrograph of an cell showing the polar associated type IV pili. A strain DZ2 (wild-type) cell is shown negatively stained with uranyl acetate.

Citation: Ward M, Zusman D. 2000. Developmental Aggregation and Fruiting Body Formation in the Gliding Bacterium , p 243-262. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch11
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Tables

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TABLE 1 Homologues and proposed functions of components of and Dif systems

Citation: Ward M, Zusman D. 2000. Developmental Aggregation and Fruiting Body Formation in the Gliding Bacterium , p 243-262. In Brun Y, Shimkets L (ed), Prokaryotic Development. ASM Press, Washington, DC. doi: 10.1128/9781555818166.ch11

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